Conserved secreted effectors contribute to endophytic growth and multihost plant compatibility in a vascular wilt fungus.

Fungal interactions with plant roots, either beneficial or detrimental, have a crucial impact on agriculture and ecosystems. The cosmopolitan plant pathogen Fusarium oxysporum (Fo) provokes vascular wilts in more than a hundred different crops. Isolates of this fungus exhibit host-specific pathogenicity, which is conferred by lineage-specific Secreted In Xylem (SIX) effectors encoded on accessory genomic regions. However, such isolates also can colonize the roots of other plants asymptomatically as endophytes or even protect them against pathogenic strains. The molecular determinants of endophytic multihost compatibility are largely unknown. Here, we characterized a set of Fo candidate effectors from tomato (Solanum lycopersicum) root apoplastic fluid; these early root colonization (ERC) effectors are secreted during early biotrophic growth on main and alternative plant hosts. In contrast to SIX effectors, ERCs have homologs across the entire Fo species complex as well as in other plant-interacting fungi, suggesting a conserved role in fungus-plant associations. Targeted deletion of ERC genes in a pathogenic Fo isolate resulted in reduced virulence and rapid activation of plant immune responses, while ERC deletion in a nonpathogenic isolate led to impaired root colonization and biocontrol ability. Strikingly, some ERCs contribute to Fo infection on the nonvascular land plant Marchantia polymorpha, revealing an evolutionarily conserved mechanism for multihost colonization by root infecting fungi.

Marchantia polymorpha model reveals conserved infection mechanisms in the vascular wilt fungal pathogen Fusarium oxysporum.

Root-infecting vascular fungi cause wilt diseases and provoke devastating losses in hundreds of crops. It is currently unknown how these pathogens evolved and whether they can also infect nonvascular plants, which diverged from vascular plants over 450 million years ago. We established a pathosystem between the nonvascular plant Marchantia polymorpha (Mp) and the root-infecting vascular wilt fungus Fusarium oxysporum (Fo). On angiosperms, Fo exhibits exquisite adaptation to the plant xylem niche as well as host-specific pathogenicity, both of which are conferred by effectors encoded on lineage-specific chromosomes. Fo isolates displaying contrasting lifestyles on angiosperms - pathogenic vs endophytic - are able to infect Mp and cause tissue maceration and host cell killing. Using isogenic fungal mutants we define a set of conserved fungal pathogenicity factors, including mitogen activated protein kinases, transcriptional regulators and cell wall remodelling enzymes, that are required for infection of both vascular and nonvascular plants. Markedly, two host-specific effectors and a morphogenetic regulator, which contribute to vascular colonisation and virulence on tomato plants are dispensable on Mp. Collectively, these findings suggest that vascular wilt fungi employ conserved infection strategies on nonvascular and vascular plant lineages but also have specific mechanisms to access the vascular niche of angiosperms.

Determinants of endophytic and pathogenic lifestyle in root colonizing fungi.

Plant-fungal interactions in the soil crucially impact crop productivity and can range from highly beneficial to detrimental. Accumulating evidence suggests that some root-colonizing fungi shift between endophytic and pathogenic behaviour depending on the host species and that combinations of effector proteins collectively shape the fungal lifestyle on a given plant. In this review we discuss recent advances in our understanding of how fungal infection strategies on roots can lead to contrasting outcomes for the host. We highlight functional similarities and differences in compatibility determinants that control the colonization of specific-cell layers within plant roots, ultimately shaping the continuum between endophytic and pathogenic lifestyle.

A 'Hydrolase Switch' for Vascular Specialization in Plant Pathogenic Bacteria.

Plant vascular diseases are tissue-specific systemic infections provoked by bacterial and fungal pathogens adapted to thrive in the xylem vessels. A recent report by Gluck-Thaler et al. reveals that, in the phytopathogenic bacterium Xanthomonas, the switch from non-vascular to vascular pathogenesis is determined by a single gene encoding a plant cell wall-degrading hydrolase.

A Conserved Microbial Motif 'Traps' Protease Activation in Host Immunity.

A recent study (Misas-Villamil et al., Nat. Commun., 2019) reveals that Pit2, an apoplastic effector of the corn smut fungus Ustilago maydis, contains an embedded motif of 14 amino acids that binds to and inhibits plant cysteine proteases, thereby modulating host immunity. Intriguingly, the inhibitory motif acts by mimicking the protease substrate and is conserved across microbial kingdoms.

Roots shaping their microbiome: global hotspots for microbial activity.

Land plants interact with microbes primarily at roots. Despite the importance of root microbial communities for health and nutrient uptake, the current understanding of the complex plant-microbe interactions in the rhizosphere is still in its infancy. Roots provide different microhabitats at the soil-root interface: rhizosphere soil, rhizoplane, and endorhizosphere. We discuss technical aspects of their differentiation that are relevant for the functional analysis of their different microbiomes, and we assess PCR (polymerase chain reaction)-based methods to analyze plant-associated bacterial communities. Development of novel primers will allow a less biased and more quantitative view of these global hotspots of microbial activity. Based on comparison of microbiome data for the different root-soil compartments and on knowledge of bacterial functions, a three-step enrichment model for shifts in community structure from bulk soil toward roots is presented. To unravel how plants shape their microbiome, a major research field is likely to be the coupling of reductionist and molecular ecological approaches, particularly for specific plant genotypes and mutants, to clarify causal relationships in complex root communities.